ABSTRACT This review examines aspects of cetacean brain structure related to behaviour and evolution. Major considerations include cetacean brain-body allometry, structure of the cerebral cortex, the hippocampal formation, specialisations of the cetacean brain related to vocalisations and sleep phenomenology, paleoneurology, and brain-body allometry during cetacean evolution. These data are assimilated to demonstrate that there is no neural basis for the often-asserted high intellectual abilities of cetaceans. Despite this, the cetaceans do have volumetrically large brains. A novel hypothesis regarding the evolution of large brain size in cetaceans is put forward. It is shown that a combination of an unusually high number of glial cells and unihemispheric sleep phenomenology make the cetacean brain an efficient thermogenetic organ, which is needed to counteract heat loss to the water. It is demonstrated that water temperature is the major selection pressure driving an altered scaling of brain and body size and an increased actual brain size in cetaceans. A point in the evolutionary history of cetaceans is identified as the moment in which water temperature became a significant selection pressure in cetacean brain evolution. This occurred at the Archaeoceti - modern cetacean faunal transition. The size, structure and scaling of the cetacean brain continues to be shaped by water temperature in extant cetaceans. The alterations in cetacean brain structure, function and scaling, combined with the imperative of producing offspring that can withstand the rate of heat loss experienced in water, within the genetic confines of eutherian mammal reproductive constraints, provides an explanation for the evolution of the large size of the cetacean brain. These observations provide an alternative to the widely held belief of a correlation between brain size and intelligence in cetaceans.

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An examination of cetacean brain structurewith a novel hypothesis correlatingthermogenesis to the evolution of a big brainPaul R. Manger*School of Anatomical Sciences, Faculty of Health Sciences, University of the Witwatersrand, 7 York Road, Parktown, 2193, Johannesburg,Republic of South Africa (E-mail: mangerpr@anatomy.wits.ac.za)(Received 5 October 2004; revised 3 January 2006; accepted 26 January 2006)ABSTRACTThis review examines aspects of cetacean brain structure related to behaviour and evolution. Major considera-tions include cetacean brain-body allometry, structure of the cerebral cortex, the hippocampal formation,specialisations of the cetacean brain related to vocalisations and sleep phenomenology, paleoneurology, andbrain-body allometry during cetacean evolution. These data are assimilated to demonstrate that there is no neuralbasis for the often-asserted high intellectual abilities of cetaceans. Despite this, the cetaceans do have volume-trically large brains. A novel hypothesis regarding the evolution of large brain size in cetaceans is put forward. It isshown that a combination of an unusually high number of glial cells and unihemispheric sleep phenomenologymake the cetacean brain an efficient thermogenetic organ, which is needed to counteract heat loss to the water. Itis demonstrated that water temperature is the major selection pressure driving an altered scaling of brain andbody size and an increased actual brain size in cetaceans. A point in the evolutionary history of cetaceans isidentified as the moment in which water temperature became a significant selection pressure in cetacean brainevolution. This occured at the Archaeoceti – modern cetacean faunal transition. The size, structure and scaling ofthe cetacean brain continues to be shaped by water temperature in extant cetaceans. The alterations in cetaceanbrain structure, function and scaling, combined with the imperative of producing offspring that can withstand therate of heat loss experienced in water, within the genetic confines of eutherian mammal reproductive constraints,provides an explanation for the evolution of the large size of the cetacean brain. These observations provide analternative to the widely held belief of a correlation between brain size and intelligence in cetaceans.Key words: intelligence, allometry, brain size, cerebral cortex, glia, marine mammals.CONTENTSI. Introduction .................................................................................................................................................II. Allometry of the cetacean brain ................................................................................................................(1) The brain-body mass relationship amongst mammals – interspecific and intraordinalcomparisons ...........................................................................................................................................(2) The brain-body mass relationship within a single species – intraspecific comparisons ...............(3) The encephalisation quotient ..............................................................................................................III. The cetacean cerebral cortex .....................................................................................................................(1) Lamination of the cetacean cerebral cortex ......................................................................................(2) Parcellation of the cerebral cortex ......................................................................................................(3) Columnar organisation of the cerebral cortex ..................................................................................(4) Neuronal morphotypes within the cerebral cortex ..........................................................................(5) Allometry of the cerebral cortex: the corticalisation index (CI) .....................................................(6) Neuronal density, the glia:neuron index, and the composition of the neuropil ...........................000000000000000000000000* Tel: +27 11 717 2497; Fax: +27 11 717 2422.Biol. Rev.: Page 1 of 46.doi:10.1017/S1464793106007019f 2006 Cambridge Philosophical SocietyPrinted in the United Kingdom1

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IV. The cetacean hippocampal formation ......................................................................................................V. Specialisations of the cetacean brain ........................................................................................................(1) Conspecific communication among cetaceans .................................................................................(2) Sleep in cetaceans .................................................................................................................................VI. Evolution of the cetacean brain .................................................................................................................VII. The intellectual capacities of cetaceans ....................................................................................................(1) Actual and relative brain size of cetaceans ........................................................................................(2) Vocalisations of cetaceans: language or simple species-specific calls? ..........................................(3) The cerebral cortex and the hippocampal formation ......................................................................(4) Does acoustic specialisation account for the increase in cetacean brain size? .............................(5) Can apparent convergences in cognitive behaviour explain the increase in cetacean brain size?VIII. Water temperature and the large cetacean brain ...................................................................................(1) Water temperature during the archaeocete/Oligocene cetacean transition ................................(2) Neuroanatomical features of the cetacean brain related to thermogenesis ..................................(3) Brain-body mass scaling in modern cetaceans and its relation to water temperature ................(4) The size of the cetacean brain ............................................................................................................(5) Evidence from other aquatic mammals .............................................................................................(a) Pinnipedia ........................................................................................................................................(b) Sirenia ...............................................................................................................................................IX. Conclusions ..................................................................................................................................................X. Acknowledgments ........................................................................................................................................XI. References ....................................................................................................................................................00000000000000000000000000000000000000000000I. INTRODUCTIONMany papers describing cetacean behaviour begin with ageneralised statement to the effect of: ‘Dolphins are re-markably intelligent creatures …’ (e.g. Tyack, 2000).Despite the high expectations placed upon the cetaceans asthe only possible ‘alien’ species with which man may have ameaningful conversation of great intellectual depth (Lilly,1962), scant evidence of this has been presented (Wu ¨rsig,2002). The compulsively anthropomorphic plurality of an-ecdotes provided in both the scientific and popular literaturecannot be considered data (Budiansky, 1998; Forestell,2002).The belief in the apparently undeniable high level ofintelligence is derived from two features of the cetaceans,one morphological and the other behavioural. The mor-phological rationale for exceptional intelligence is the largesize and gyrencephalic nature of the brain (Fig. 1). Indeed,cetaceans have large brains, with some species having thelargest brain of all animals, weighing in excess of 8 kg (Pilleri& Gihr, 1970). Humans also have large brains, which werecognise to be the basis of our intellectual capacities. Onevery influential view regarding the evolution of brain sizeis the relationship forwarded by Jerison (1973), that residualbrain size (that remaining from a correction for body size) isa determinant of biological intelligence. Thus, the generalconclusion is: large relative brain size equals great intelli-gence. This hypothesis has been attached to the cetaceans asproof of some form of extraordinary intelligence (Jerison,1978). Perhaps unwittingly, Jerison has asserted that therecan be only one reason for the brain to increase in relativesize – an adaptive increase in its information-processingcapacity, i.e. increased intelligence.This assertion, which has been selectively examined in thecase of cetaceans, and of which there is contradictory pub-lished data (e.g. the baleen whales have some of the lowestmammalian encephalisation quotients, so are they, despitehaving brains weighing several kilograms, therefore some ofthe most unintelligent mammals?), is the maxim for manystudies of cetacean brain and behaviour. However, it ispossible that increases in relative and actual brain size arenot always adaptive responses to a need for greater infor-mation processing capacity but that brain size increases area response to an alternative selection pressure. The presentpaper deals with this issue in regard to the evolution of brainsize in cetaceans.The second feature commonly construed to provide evi-dence of high intellectual capacities in the cetaceans is thevocal proclivity of this mammalian order. Language, dia-lects, conversations, grammatical competency, and severalother human linguistic terms are often used to describe thevocalisations of cetaceans. All attempts to teach dolphins animposed language are based upon stimulus-response be-havioural paradigms (or operant conditioning) (Herman &Tavolga, 1980; Herman, 2002) – a basic form of learning(Thomas, 1996). At best, dolphins have been shown to becapable of learning approximately 40 symbolic associations(or ‘words’) (Herman & Tavolga, 1980; Herman, 2002).Other work has concentrated upon deciphering ‘dol-phinese’, i.e. the vocalisations themselves. However, studiesof dolphin vocal repertoires have shown that they are limitedto approximately seven (range 5–20) different characteristicsounds (Herman & Tavolga, 1980). The vocalisations arenotacomplexinterwoventapestryprovidingabasisforcom-munication of thoughts and feelings, and they do not exhibitthe higher order entropies typical of human language2Paul R. Manger

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Fig. 1. (A) Photograph of the lateral surface of the killer whale (Orcinus orca) brain. Scale bar=1 cm. (B) Photograph of a coronalslice through the brain of a piebald dolphin (Cephalorhynchus commersonii). Scale bar=1 cm. The deep and convoluted sulci arecharacteristic of all cetacean brains. The sulci and gyri of the cetacean have the appearance of those found in human patientssuffering from micropolygyria (Welker, 1990). The brains photographed here are from the collection of Dr Sam H. Ridgway.Cetacean brain evolution and thermogenesis3

(McCowan, Hanser & Doyle, 1999). Rather, these seventypical vocalisations appear to be seven different species-specific calls, such as has been seen in many other animals,some of which have far more calls than the seven typicallyfound for bottlenose dolphins. In summary, it appears thatthe evidence in favour of significant intellectual capacitiesof dolphins is tenuous, and based upon untested, unproven,unquestioned, and anthropomorphic assumptions.The present paper provides a critical review of cetaceanbrain structure in comparison to the brain of other mam-mals. No invasive experiments of the cetacean brain havebeen undertaken in the modern era of neuroscience dueto the Marine Mammal Protection Act; thus the only wayto decipher cetacean brain function is from comparativeinformation garnered from laboratory animal experimen-tation and compare this to post-mortem cetacean tissue.Observations on cetacean brain structure presented here arederived from sources in the literature and primary obser-vations. Cetacean brain allometry is reanalysed and com-pared to both extant and extinct mammals, and to theenvironment of the various cetacean species. The allometryand structure of the cerebral cortex is reviewed in light ofseveral recent and older studies demonstrating an atypicalstructure of the cerebral cortex in cetaceans. Two speciali-sations of the cetacean brain are described, which relate tothe vocalisations and sleep physiology of the cetaceans. Theevolution of the cetacean brain is traced by comparing fossilendocasts of extinct cetacean species with those of moderncetaceans. These data are assimilated to provide a neuro-anatomical basis indicating that cetaceans lack sophisticatedcognitive abilities. Finally, a data-based hypothesis is for-warded suggesting that the evolution of large brain sizein cetaceans is an adaptation to a thermally challengingenvironment.II. ALLOMETRY OF THE CETACEAN BRAIN(1) The brain-body mass relationship amongstmammals – interspecific and intraordinalcomparisonsThe allometric relationship between brain mass and bodymass in vertebrates has been calculated, recalculated, andspeculated upon for well over a century (reviewed in Jerison,1973). It is clear that a significant, statistically reliable pre-dictor of brain mass across the majority of vertebrate speciesis body mass, although the reasons for this are still specu-lative (Armstrong, 1990; Harvey & Krebs, 1990). Threetypes of allometric calculations are generally undertaken,those comparing species’ averages from a range of orders(interspecific), those comparing species’ averages from thesame order (intraordinal), and those comparing data fromindividualswithin thesame(Armstrong, 1990). The first two of these comparisons areconsidered in this section, the latter in the next section.Several studies have examined the brain mass versus bodymass relationship of cetaceans (e.g. Pilleri & Gihr, 1970;Jerison, 1978), and a reanalysis of this relationship with ad-ditional data and a new perspective is undertaken here.species (intraspecific)Brain mass and body mass data were taken from severalpublished sources, for cetaceans (see Table 1), and othermammals (Bininda-Emonds, Gittleman & Kelly, 2001;Crile & Quiring, 1940; Stephan, Frahm & Baron, 1981;Wood & Collard, 1999). Allometric equations using least-squares regression analysis were calculated for five groups:odontocete cetaceans, odontocete combined with mysticetecetaceans, hominids, primates, and the remaining mammals(Fig. 2). The division of the analysis into these five groupswas done for the following reasons. Firstly, the majority ofmammals show a similar brain-body scaling across species,thus, it is most efficient to deal with these data as an inter-specific comparison, to provide a baseline for comparison tothe species of interest. An intraordinal analysis was used forprimates (excluding the hominids), as it is clear from pre-viously published material that this group, while scaling in asimilar manner to other mammals, does have a substantiallydifferent brain mass: body mass ratio. An intrasubordinalanalysis was appropriate for hominids because of the dra-matic difference in scaling of this suborder in comparison toother primates. Finally, an intraordinal analysis of the cet-aceans, and intrasubordinal analysis of the odontocetes wereused, as in both cases the species within this order have adifferent brain mass: body mass scaling compared to that ofother mammals.In the present analysis, the plot of brain (Mbr) versus bodymass (Mb) for mammals in general (excluding cetaceans andprimates) gave results similar to those previously published(e.g. Armstrong, 1990; Harvey & Krebs, 1990). The al-lometric equation calculated was:Mbr=0:069M0:718b(r2=0:950; P=2:4r10x178):(1)Note from equation (1) that the slope of the line (0.718) andthe constant k (0.069) are in agreement with several previousstudies (see references in Armstrong, 1990 and Harvey &Krebs, 1990). Also, the correlation coefficient is extremelyhigh, thus, for most mammals 95% of the variability in brainmass can be accounted for by the variability in body mass.The equation calculated for primates (excluding homi-nids) is:Mbr=0:100M0:756b(r2=0:939; P=6:1r10x50):(2)The slope of this regression (0.756) reflects a similar patternof scaling of primate brain mass versus body mass whencompared with other mammals, but primates appear tohave a greater brain mass relative to body mass than mostmammals (as reflected in the higher constant, k=0.100).Again r2is high, with 94% of the variability in brain size ofprimates being accounted for by changes in body size.The scaling of brain mass and body mass in hominidspecies, both extinct and extant is given by:Mbr=0:000003M1:793b(r2=0:867; P=0:00016):(3)The slope of the line (1.793) appears steeper than that seenfor mammals (equation 1) and primates (equation 2)(although P=0.059 using the mean squares between andwithin slopes, indicating that while the slopes calculatedby the regression analysis are not statistically different, theP value is close to significance, possibly as a result of the6Paul R. Manger

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small sample size for hominids compared to mammals); r2is lower so that for hominids, only 87% of the variability inbrain mass can be accounted for by body mass variation.For the odontocetes the regression equation is:Mbr=3:426M0:469b(r2=0:793; P=1:1r10x11), (4)and for all cetacean species (odontocetes+mysticetes):Mbr=10:116M0:376b(r2=0:812; P=3:7r10x14):(5)For odontocetes, the slope of the line, at 0.469, is signifi-cantly less steep than that of the other mammalian groupsexamined (P=1.6r10x8, using the mean squares betweenFig. 2. (A) Plots of the raw data of brain (Mbr) and body mass (Mb) of a variety of mammalian species. The present analysisexamined four groups, mammals in general (black circles), primates (open circles), hominids (open squares), and cetaceans (odon-tocetes – triangles, mysticetes – stars). (B) Regression lines and allometric equations of the various groups examined in the presentanalysis. Note the altered scaling for both hominids and cetacean species from that seen for mammals and primates. The data usedin this plot are derived mainly from Crile & Quiring (1940), and other sources listed in Table 1.Cetacean brain evolution and thermogenesis7

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and within slopes). For all cetaceans (equation 5), the slopeflattens even more, at 0.376 (comparison with the other fourgroups using the mean squares between and within slopesP=9.1r10x26). Note that cetaceans vary from the generalmammalian, or primate brain-body mass scaling in the op-posite direction to the trend shown by hominids. For theodontocete cetaceans and all cetaceans, only 80% or 81%,respectively, of the variability in brain mass can be ac-counted for by variability in body mass.These calculations indicate that the brain mass versus bodymass relationship in cetaceans differs significantly from thatfor other mammals while the hominid data also suggest adifferent trend (see above). Analyses of individual orders ofmammals give slopes in the range of 0.55–0.66 (see theevolutionary analysis of ungulates in Section VI and Fig. 12;and the results of the studies referenced in Armstrong,1990). We can conclude that while there is a trend for in-creasing brain size with increasing body size in cetaceansand hominids, in accordance with the general trend inmammals (and indeed in other vertebrates), there mustbe additional factors causing the observed differences inscaling. The altered scaling of cetaceans is in the oppositedirection to the trend seen in hominids, and while cetaceansare fully aquatic, hominids have remained terrestrial, thus, itseems likely that different selection pressures acted uponcetaceans and hominids leading to the observed scaling inthese groups.(2) The brain-body mass relationship within asingle species – intraspecific comparisonsIntraspecific comparisons have shown that the brain-bodymass scaling within a single species is quite different tothat of intraordinal and interspecific scaling with a meanslope of 0.22 (see Armstrong, 1990, and references listedtherein). Thus, an individual twice the body mass of aconspecific is likely to have a brain 20.22, or 116.47%, larger.This scaling has been found in a range of mammalianspecies, including humans, various primates, moles, dogs,sheep, pigs, raccoons and ferrets (see references inArmstrong, 1990). The curious exception to this generalconsensus is the domestic cat, where the slope was 0.67,closer to the intraordinal or interspecific scaling values(Bronson, 1979).While intraspecific analyses of cetacean species areavailable (Pilleri & Gihr, 1970), a reanalysis of these datawith additional data from other publications (e.g. Ridgway,1990) is undertaken here. Only data judged to be reliableare used, thus, individual data points that lie grossly outof the normal range of the adult, presumably indicatingeither a juvenile or sick animal, were excluded. Moreover,data where body mass was estimated rather than measured,such as for the larger cetaceans, were also excluded.Intraspecific analyses were undertaken on Lagenorhynchusalbirostris,Stenella coeruleoalbaPhocoenoides truei, Delphinus delphis, and Tursiops truncatus [datafrom Pilleri & Gihr (1970) except Tursiops truncatus whichwere from Ridgway (1990)]. Allometric equations, as de-scribed above, were calculated for each of these species(Fig. 3).These allometric equations have slopes ranging between0.329 and 0.728, which appear to differ from the slope of0.22 found for the majority of mammalian species pre-viously studied (Armstrong, 1990). In the above intraordinalanalyses of the odontocetes (eq. 4) and all cetaceans (eq. 5),the slopes were 0.469 and 0.376. The intraspecific allometric(formerlyStenellastyx),Fig. 3. Intraspecific scaling of brain mass (Mbr) versus body mass (Mb) for five cetacean species. Data are derived from Pilleri & Gihr(1970), and Ridgway (1990).8Paul R. Manger

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slopes are very close to these values, with one exception, thatof Phocoenoides truei, where the slope was 0.728. The range ofslopes, and lower correlation coefficients, found in the in-traspecific analysis may be due to the small data sets.However, to a first approximation the general trend forintraspecific scaling of brain and body mass in cetaceanspecies is similar to that found for the intraordinal allometricscaling (in all cases the calculated regression slopes for indi-vidual cetacean species are not significantly different to thatof the slope calculated for odontocetes using the meansquares between and within slopes: T. truncatus vs odonto-cetes, P=1; D. delphis vs odontocetes, P=1; P. truei vsodontcetes, P=1; S. coeruleoalba vs odontocetes, P=1;L. albirostris vs odonocetes, P=1).It has been proposed that: ‘If species-specific differencesarose through natural selection, one obvious hypothesis isthat individual differences within a species would havethe same slope, so that selection for a bigger body (or brain)would scale the correlated feature to the appropriatesize.’ (Armstrong, 1990). This clearly is not the case formost mammals (Armstrong, 1990); however, the scalingof intraspecific differences in brain and body mass in cet-aceans is similar to the intraordinal scaling of these species.It is therefore likely that natural selection, via a specificselection pressure, initiated the altered scaling of brainand body in cetaceans, and that this selection pressurecontinues to influence brain-body scaling in extant cetaceanspecies. Thus, identification of a selection pressure in-fluencing the scaling seen in extant cetaceans could alsoexplain the evolution of the difference in scaling of the entireorder.(3) The encephalisation quotientJerison (1973) suggested that the encephalisation quotient(EQ), i.e. the relative amount of brain per unit body size, canbe used as a direct estimate of the intelligence of a species.This use of the EQ is encapsulated by Gibson (2001, p. 3):‘In Jerison’s framework, mammals were the most intelligentvertebrates, and those mammals whose brain size exceededthe predicted brain size of other mammals of similar bodysize were the most intelligent mammals.’ While a superficialexamination of the data seems to fit intuitive reasoningconcerning the intellectual abilities of certain species, thisproposal has not stood up to scrutiny as a measure of bio-logical intelligence (Harvey & Krebs, 1990). Despite this, themodern literature on cetacean brain-body allometry stilluses the EQ as cause for speculation on the intellectual ca-pacities of cetaceans (e.g. Marino, 1998).I have recalculated the EQs of all cetaceans using theallometric equation obtained for most mammals (eq. 1). Thechoice of a reference group is a much-debated issue in thestudy of allometry (Bauchot & Stephan, 1966; Jerison,1973; Stephan et al., 1981), however, as we are investigatingdifferences between cetaceans and other mammals, the useof equation (1) is appropriate. The EQs of cetaceans (Fig. 4)show that some species have large EQs (second only tohumans) while some have very low values (lower than theaverage mammalian EQ of 1). The range of values seen isnot surprising, as the slope of the allometric equation forbrain mass: body mass for cetaceans (Fig. 2B) is quite shal-low, intersecting the regression lines derived for mostmammals and for primates. The raw data plot (Fig. 2A),shows that some cetaceans fall well above the regressionlines for most mammals and primates, while some are wellbelow.The calculation of the EQ is a relatively simple matterand, to an extent, the conclusions drawn are dependent onthe species included in the data set. For example, Marino(1998) calculated the EQ of odontocete cetaceans, however,did not include published data for several key odontocetespecies. The exclusion of such species as Physeter catadon,which has both a large brain and body mass is likely to alterthe outcome of this analysis: the slope calculated for thebrain: body mass scaling of odontocetes by Marino (1998) is0.53, which is statistically similar to that found in the presentstudy: 0.469, equation (4) [comparison of the regressionslopes calculated for the data of Marino (1998) comparedwith that used in the present study for odontocetes only re-vealed no significant difference (P=0.275) using the meansquares between and within slopes]. The inclusion of themysticetes into the regression analysis leads to a significantshallowing of the slope of the regression: 0.38, equation (5)[comparison of the regression slopes calculated for the dataof Marino (1998) compared with that used in the presentstudy for all cetaceans revealed a significant difference(P=0.029) using the mean squares between and withinslopes]. Conclusions regarding ordinal encephalisation lev-els should aim to include as many data points as possible.Marino (1998) only included odontocetes with similar brainmass: body mass ratios to the anthropoid primates (see Fig.1 in Marino, 1998). Not surprisingly therefore Marino(1998) concludes: ‘… the gap between human and non-human levels of encephalisation (and, in a general way, in-telligence) is substantially narrowed by a nonprimategroup …’. Marino (1998) goes on to assert that cetaceans,especially the highly encephalised Delphinidae, are secondonly to humans in intelligence. While the EQ is a usefulallometric measure (see Section VIII), it is difficult to resolvethis as a measure of biological intelligence as proposed byFig. 4. Bar graph of the encephalisation quotients (EQs) ofextant primates and cetaceans.Cetacean brain evolution and thermogenesis9

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Jerison (1973). The high EQ values found in some cetaceansmay simply be due to the altered allometric scaling of brainand body masses.III. THE CETACEAN CEREBRAL CORTEXThe cerebral cortex is the most complex information-processing station in the brain of all mammals. It is thoughtto be central to many major processes, such as intra- andinter-sensorial perceptual binding, and long-term memory,and is believed by many to be essential for complex cogni-tive behaviours.(1) Lamination of the cetacean cerebral cortexSeveral previous studies have described the cytoarchi-tectural features and lamination of the cerebral cortex ofcetaceans. The majority of these reach conclusions that donot differ from much earlier examinations (Major, 1879).A brief overview of the cytoarchitecture of the cetaceancerebral cortex is provided here with representative ex-amples shown in Fig. 5.Fig. 5. Nissl-stained sections of the cerebral cortex in three cetacean species from different families. Cortical layers 1–3, 5 and 6 areidentified in B and E. A–C are from putative primary visual cortex (V1); D–F are from putative primary auditory cortex (A1). A andD are from a beluga whale (Delphinapterus leucas, brain mass 2083 g), B and E from a pilot whale (Globicephala melas, brain mass 2673 g),and C and F from a goose-beaked whale (Ziphius cavirostris, brain mass 2004 g). Features of the cetacean cortex, such as a lack of thegranular layer 4, poor columnar organisation, thick layer 1, unclear lamination of layers 3 to 6, low cellular density, and high gliadensity, among others, are evident in these sections of primary sensory cortex. Scale bar=500 mm, applies to all panels. Thephotomicrographs used in this figure were generously supplied by Patrick Hof from the Morgane-Jacobs-Glezer marine mammalbrain collection.10Paul R. Manger

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Several authors comment upon the thickness of layer 1across the entire cetacean cerebral cortex (e.g. Haug, 1987;Hof et al., 2000; Kesarev, Malofeyeva & Trykova, 1977;Kojima, 1951; Revishchin & Garey, 1991). Layer 2 isgenerally acknowledged to be the most cell-dense, thinnest,and distinct layer in the cetacean cerebral cortex. More-over, it is regularly reported that the majority of neuronsin layer 2 are pyramidal in nature, with a scarcity ofgranular neurons, i.e. a ‘pyramidalisation’ of layer 2 hasoccurred (e.g. Kojima, 1951; Manger et al., 1998; Pilleri &Gihr, 1970). Layer 3 is a relatively thick cortical layerin cetaceans, and is composed of a moderate density oflarge pyramidal cells. The size of the pyramidal cells in-creases with depth in this layer (Kojima, 1951), and someauthors have described sublamina on this basis (Morgane,Glezer & Jacobs, 1988). Almost all authors agree that layer 4is either absent or extremely underdeveloped (e.g. Breath-nach, 1960; Glezer, Hof & Morgane, 1998; Hof et al., 1994,2000; Kesarev et al., 1977; Kojima, 1951; Morgane et al.,1988). Glezer, Jacobs & Morgane (1988) describe layer4 as ‘incipient’. Layer 5 appears to show little regionaldifferences in thickness. It is especially prominent in themotor region of the cortex, due to the giant cells ofBetz. However, the border between layers 3 and 5 isoften described as indistinct (e.g. Breathnach, 1960; Kesarevet al., 1977; Kojima, 1951). Layer 6 is also found in allregions of the cortex and is made up of several neuronaltypes including scattered large pyramidal, round and stellateneurons (e.g. Breathnach, 1960; Kesarev et al., 1977;Kojima, 1951).Three points of interest emerge from the above: thelamination of the cetacean cerebral cortex is not distinct;layer 2 exhibits ‘pyramidalisation’; and layer 4 appears tobe largely absent. Various names have been given to thetype of cerebral cortex exhibited by the cetaceans; however,Brodmann’s (1909) terminology appears most appropriate.On the basis of the lack of layer 4, cetacean cerebral cortexis a ‘heterotypical formation’ resulting from a reduction inthe number of cortical layers. This is supported by the ob-servation of a thin layer 4 in the visual cortex of the bottle-nose dolphin during development (Garey & Leuba, 1986).Brodmann (1909) also noted the pyramidalisation (Pilleri &Gihr, 1970), or the ‘secondary transformation’, of the neur-onal elements of layer 2 in various species of mammals. Thelaminar organisation of the cetacean cerebral cortex shouldthus be considered a heterotypical formation in which layer2 has undergone a secondary transformation specific to theCetacea.(2) Parcellation of the cerebral cortexAn increase in the number of cortical areas is commonlythought to reflect an increase in behavioural complexity.Kaas (1995) stated that: ‘… the functioning of large brainsmay be enhanced by having more subdivisions’. The num-ber and organisation of cortical areas in several species ofmammals has been studied, however, few attempts havebeen made to subdivide the cortex of the cetaceans.Subdivision of the cortex can be assessed using severaltechniques; however, those used on the cetacean cortex arelimited to cytoarchitectural analysis and a small amount ofelectrophysiological mapping.The large surface area of the cerebral cortex of the cet-aceans makes parcellation a daunting task, especially underthe generally accepted paradigm that larger brains are com-posed of more sensory subdivisions (Kaas, 1995). However,several studies have localised regions of bottlenose dolphinneocortex using cytoarchitectural techniques (Garey &Leuba, 1986; Kesarev et al., 1977; Kojima, 1951; Mangeret al., 1998; Morgane et al., 1988) and electrophysiologicalrecording (Bullock & Gurevich, 1979; Ladygina, Mass &Supin, 1978; Lende & Akdikmen, 1968; Lende & Welker,1972; Sokolov, Ladygina & Supin, 1972). These provide areasonable degree of detail regarding localisation of areaswithin the bottlenose dolphin cortex (Fig. 6).Kesarev et al. (1977) describe six major cytoarchitectonicregions within the dolphin neocortex (Fig. 6A–D). Theseregions are in turn subdivided into one or more cytoarchi-tectonic fields. Physiological observations have provideddetails of the locations of sensory projection areas in theneocortex, these being visual and auditory (Ladygina et al.,1978; Sokolov et al., 1972) and somatosensory and motorareas (Lende & Akdikmen, 1968; Lende & Welker, 1972)(Fig. 6E–H). There appears to be good correlation betweenthe cytoarchitectural and electrophysiological observations.Kesarev et al. (1977) describe a region of cortex that theyterm occipital (O), located on the occipital and posteriormidline cortex. This region corresponds to regions of cortexresponsive to visual stimulation (Ladygina et al., 1978;Sokolov et al., 1972). Kesarev et al. (1977), Morgane et al.(1988) and Sokolov et al. (1972) describe three cytoarchitec-tonic fields within this region, one of which probably corre-sponds to primary visual cortex (described as medialoccipital area, Om; heterolaminar; and short latency, re-spectively in these three publications). Photomicrographs ofsections through this region suggest that layer 4 may bepresent although cells that are granular in appearance areinterspersed within lower layer 3 and upper layer 5 (Kesarevet al., 1977). The second cytoarchitectonic field (described assuperior occipital, Os; homolaminar; and long latency,respectively) may correspond to extrastriate visual cortex;however, this region has not been subdivided into multipleareas as in other mammalian species, as no further studieshave examined this region of the cetacean cortex. The thirdcytoarchitectonic field, the borderline medial occipital area(Olm), lies in a position postero-medial to the Om, and exhi-bits an architecture that indicates that it might correspond tothe splenial visual area of other mammals (assuming thatOm is primary visual cortex) (Rosa, 1999).Lateral to the occipital cortex, Kesarev et al. (1977)describe a large region of dorsal surface cortex, which theyterm parietal cortex (P). This region corresponds with theregion known to be responsive to auditory stimulation(Ladygina et al., 1978; Sokolov et al., 1972). This P regionhas been subdivided into four cytoarchitectonic fields(superior parietal Ps, medial parietal Pm, inferior parietalPi, and transitional parietal Pli), each of which is likely torepresent an auditory cortical area. It is unclear whichcytoarchitectonic field represents primary auditory cortexand which are secondary or tertiary auditory areas.Cetacean brain evolution and thermogenesis11

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Fig. 6. Parcellation of the cetacean cerebral cortex demonstrating the architectonic and physiological subdivisions of the cerebralcortex of the bottlenose dolphin. A–D are redrawn from the architectonic subdivisions of Kesarev et al. (1977). The regions arelabelled according to the original publication as follows: Cl, central lateral area; Cm, central medial area; Fl, frontal lateral area;12Paul R. Manger

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Lateral and posterior to both the occipital and parietalregions of cortex is an underdeveloped wedge-shaped pieceof cortex termed temporal cortex (T) by Kesarev et al.(1977). This is likely to correspond to the temporal cortexof other mammalian species, an assumption based on itslocation relative to the visual and auditory regions. It iscomposed of two cytoarchitectonic fields, the internal tem-poral area (Ti) and the external temporal area (Te). Anteriorto both the occipital (visual) and parietal (auditory) regionsof cortex lies a region designated as central (C) by Kesarevetal.(1977).Thisregioncorrespondstotheregionsresponsiveto somatosensory stimulation (Ladygina et al., 1978; Lende& Welker, 1972; Sokolov et al., 1972) and that producingmotor actions upon electrical stimulation (Lende &Akdikmen, 1968). Kesarev et al. (1977) described centrallateral (Cl) and central medial (Cm) cytoarchitectonic fields;Cl appears to correspond to somatosensory cortex and Cmto primary motor cortex. The Cm region appears to corre-spond to the region designated primary motor cortex in thesperm whale by Kojima (1951) (Fig. 7), due to the presenceof Betz cells (Kesarev et al., 1977).Anterior to central cortex (somato-motor cortex) is a smallregion designated frontal (F) by Kesarev et al. (1977). Thisregion is composed of frontal lateral (Fl) and frontal medial(Fm) cytoarchitectonic fields, and is located on the mostanterior pole of the cerebral cortex. On topological grounds,one might be tempted to designate this region prefrontalcortex; however, several observations indicate that this isprobably not the case. The exact definition of prefrontalcortex across mammals is a complex and much debatedissue (e.g. Divac & O¨berg, 1990; Preuss, 1995); however,this debate may be avoided by a closer examination of thecytoarchitecture of this region. The feature of most interestis the presence of numerous giant pyramidal cells in thisregionofcortex(dolphin – Langworthy,1932;Kesarevetal.,1977; sperm whale – Kojima, 1951) (Fig. 7). These cellsexist in primary motor cortex and premotor cortex of otherspecies of mammals (Brodal, 1968, 1978, 1980) (Fig. 7), andgive rise to the cortico-pontine projection. They are notfound in prefrontal cortex. This observation suggests thatthis region of cortex is premotor cortex, and stimulationof this region does produce motor movements (Lilly, 1962).One must note that this cytoarchitectonically distinct regionof cortex extends to the most anterior portion of the cerebralcortex, thus, if there is a region of cortex that may be definedas prefrontal in the cetaceans, it is very small.On the medial surface of the hemisphere, located be-tween the corpus callosum and the cingulate sulcus, is theregion of cortex defined as limbic cortex (L) by Kesarev et al.(1977) (Fig. 6). Compared to other mammals, this region ofcortex is rather reduced in size, and probably corresponds tocingulate cortex. Kesarev et al. (1977) describe five cyto-architectonic fields in this region but also note the ratherhomogeneous nature of this cortex. Finally, on the medialbank of the insular cortex, entorhinal cortex has beenlocated, in a topological position that is consistent withits location in other mammals (Manger et al., 1998).The assignations of the cortical regions given above areconsistent with studies of thalamocortical connectivity incetaceans (Revishchin & Garey, 1990). Within the realms ofinterspecies comparisons, it therefore appears that theoverall topology of the areal subdivision of cerebral cortex incetaceans does not differ dramatically from that seen inother mammals. However, four points of importanceemerge: there does not appear to be a prefrontal corticalregion; the number of subdivisions of the cortex appears tobe low compared with other mammals with similarly sizedbrains or even mammals with far smaller brains; the tem-poral cortical region is small and undeveloped; and thelimbic region of cortex, or cingulate cortex, is small,especially in its anterior aspect.(3) Columnar organisation of the cerebral cortexVertically oriented columnar structures within the sensorycerebral cortex have been identified in a range of mam-malian species. These include several distinct types, from thephysiological columns first described by Mountcastle (seereview by Mountcastle, 1997), that often correspond toanatomically identifiable modules (e.g. Manger et al., 1998),to the microcolumns (or minicolumns) that make up thelarger cortical columns (Jones, 2000). These radially or-ganised columns cross layer boundaries and are thought torepresent the fundamental processing units of the sensorycerebral cortex. In cetaceans, visually identifiable corticalcolumnar organisation has only been reported in theentorhinal cortex of the bottlenose dolphin (Manger et al.,1998). It is difficult to identify columnar and microcolumnarorganisation in the photomicrographs of architectonicallydefined regions of dolphin brain provided by Kesarev et al.(1977), whereas these features are readily identifiable in thecortex of other mammals (Jones, 2000; Manger et al., 1998;Fm, frontal medial area; La, anterior limbic area; Lla, anterior borderline area; Llp, posterior transitional, or borderline, limbicarea; Lp, posterior limbic area; Ls, anterior subgenual area; Olm, borderline medial occipital area; Om, medial occipital area; Os,superior occipital area; Pi, inferior parietal area; Pli, transitional parietal area; Pm, medial parietal area; Ps, superior parietal area;Te, external temporal area. (E) The approximate locations of primary somatosensory (S1) and primary motor (M1) cortex from themapping studies of Lende & Akdikmen (1968) and Lende & Welker (1972). Note the correspondence of the partial maps to the areastermed Cl and Cm by Kesarev et al. (1977). (F) Architectonic and physiological locations of visual cortex from the studies of Morganeet al. (1988) and Sokolov et al. (1972). It appears that the heterolaminar and short latency regions correspond to V1 of othermammals. Note the correspondence between these regions and the regions termed Os and Om by Kesarev et al. (1977). (G, H)Physiological subdivisions of dolphin cerebral cortex from Ladygina et al. (1978). Note the correspondence of the visually responsivecortex to regions Os, Om and Olm, auditory to regions Pi, Pli, Pm and Ps, and somatosensory to Cl, in the scheme of Kesarev et al.(1977). The location of entorhinal cortex is from Manger et al. (1998). Scale bar in C applies to all panels.Cetacean brain evolution and thermogenesis13

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Mountcastle, 1997). Despite this Morgane et al. (1988)identified two radially oriented columnar structures in dol-phin visual cortex using computer-assisted methods: minorcolumns with diameters of around 20 mm, significantlysmaller than the mean of 56 mm found in other mammals(Mountcastle, 1997); and major columns, approximately168 mm diameter, which are again smaller than the corticalcolumns or modules (range 250–1000 mm) found in thecortex of other mammals (Manger et al., 1998). Morganeet al. (1988) note that these columns are often discontinuousacross the cortical layers.(4) Neuronal morphotypes within thecerebral cortexOne major feature of the mammalian cerebral cortex is thediversity and complexity of the neuronal morphology.Several studies have found a low diversity of neuronal typesFig. 7. The location of the giganto-pyramidal cells that indicate the origin of the cortico-pontine tract in the macaque monkey(Brodal, 1978, 1980), domestic cat (Brodal, 1968), and sperm whale (Kojima, 1951). Note the high density of these cells in primarymotor cortex (M1) and the moderate density in premotor cortex (Pre-M). None of these cells are seen in prefrontal cortex of themacaque monkey or domestic cat. However, there appears to be no region anterior to the origin of the corticopontine tract in thesperm whale that would indicate the presence of a prefrontal cortical region.14Paul R. Manger

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in the cerebral cortex of odontocete cetaceans. These studiesconfirm that the majority of cortical neurons are pyramidalin nature, they have a few simple shapes, and there is sparseramification of the dendrites (Kesarev, 1971; Kesarev et al.,1977; Glezer et al., 1988; Morgane, Jacobs & Galaburda,1985; Morgane et al., 1988; Morgane, Glezer & Jacobs,1990). An interesting feature to emerge from these studiesis the presence of extraverted pyramidal neurons in layer 2.These neurons exhibit a dendritic ramification into layer 1and, by comparison with other pyramidal neurons of cet-acean cerebral cortex, are quite spinous. These neurons arenot a common feature of the cerebral cortex of othermammals. The majority of pyramidal neurons in the cet-acean cerebral cortex exhibit triangular, club-shaped orclavate-type soma, which are thought to indicate a poordegree of differentiation(Morgane et al., 1990).Non-pyramidal, or stellate, cells make up around 12% ofthe neuronal population in odontocete cetacean cortex(Morgane et al., 1985). The majority of these neurons areof the long-radiator type, which is thought to representan undifferentiated neuronal morphology (Morgane et al.,1990). Stellate neurons of the short-radiator type have beenreported only occasionally (Morgane et al., 1985, 1990).In a series of studiesHofet al.(1999, 2000) and Glezer etal.(1998) used calcium-binding protein immunohistochemistrytoexaminetheinhibitorycomponentofthecetaceancorticalnetwork. Many neurons immunoreactive for the calcium-binding proteins, calbindin, calretinin and parvalbumin arealso immunoreactive for c-aminobutyric acid (GABA) andare thus considered to be inhibitory. Cetaceans have a highproportion of calbindin- and calretinin-immunoreactiveneurons compared to those showing parvalbumin im-munoreactivity (approximately 4:1), whereas the ratio iscloser to 1:1 in primates and rodents (Hof et al., 1999, 2000;Glezer et al., 1988). However, cetaceans have almost twice asmanyoftheseneuronsasprimatesandrodentswhentheyareexpressed as a proportion of total neuronal number (Hofet al., 2000). In cetaceans, calbindin- and calretinin-immunoreactive cells are found mostly in the upper corticallayers, while parvalbumin-immunoreactive cells are locatedin the lower cortical layers. The diversity in neuronalmorphologies of these inhibitory neurons is low in cetaceanscompared to many other mammals (Hof et al., 1999).Calbindin- and calretinin-immunoreactive neurons havebeen implicated in the flow of inhibitory influences in thevertical dimension in cerebral cortex, i.e. within a corticalcolumn, and parvalbumin-immunoreactive cells function inhorizontal inhibitory flow, i.e. between cortical columns.Thehighproportionofimmunoreactive cells in cetacean cerebral cortex suggestsmarked vertical inhibitory influences. This, combined witha low diversity in neuronal morphology, might indicate ahigh degree of monotonous specificity in vertical infor-mation processing, which might be seen as indicative ofdetailed perceptual abilities. By contrast, the relative paucityof parvalbumin-immunoreactive cells indicates a lack ofhorizontal inhibitory influences, potentially characterizinginefficient horizontal processing between cortical columns,and suggesting poor integrative abilities.ofneuronalmorphologiescalbindin-and calretinin-(5) Allometry of the cerebral cortex: thecorticalisation index (CI)Glezer et al. (1988) used the percentage of the total brainvolume that is cerebral cortex [the corticalisation index (CI)]to assess the relative size of the cerebral cortex in cetaceans.They compared the CI of bottlenose dolphin against twospecies of insectivores and six primates and found that theCI of the bottlenose dolphin was significantly smaller thanthat of these other mammals.I have repeated this analysis with the addition of futherspecies (see Table 2), and calculated the CI using two dif-ferent methods. First, the CI was calculated as the totalcombined volume of the grey and white matter of the cer-ebral cortex expressed as a percentage of brain volume.Fig. 8A shows the CI calculated using this method plottedagainst brain volume. Using this method, we see that thecetaceans show similar CIs to those of the simian primates.The average CI for simian primates was 70.22% (range66.09–84.02%), and for odontocete cetaceans 72.14%(range 70.39–73.40%). Both these groups cluster abovethe average and range found for other mammals (average45.81%,range22.18–63.96%),(average 49.57%, range 33.87–59.55%), and insectivores(average 23.67%, range 11.84–57.31%). This analysisindicates that the amount of the odontocete brain devotedto grey and white matter of the cerebral cortex is compar-able to that in simian primates, but greater on averagethan that seen in prosimians, other mammals and in-sectivores.In the second method CI was calculated as the volumeof the grey matter of the cerebral cortex expressed asa percentage of brain volume (see Table 2 and Fig. 8B).Using this method, a slightly different picture emerges.The simian primates have an average CI of 52.69% (range49.17–56.07%), while the odontocete cetaceans have anaverage CI of 40.56% (range 36.14–42.44%). Thus, thissecond method separates the odontocete cetaceans from thesimian primates. Moreover, they average less than the othermammals (average 47.29%, range 40.13–56.73%) includedin this analysis, and the one prosimian used (CI=49.08%),but higher than the insectivores (average 28.49%, range26.31–30.03%). The single mysticete for which data wasavailable had a CI of 20.53%.These two analyses offer somewhat contradictory views.Using the first method, the odontocete cetaceans group withthe simian primates, indicating that in these two groups,similar amounts of the total brain volume is devoted to thegrey and white matter of the cerebral cortex. But whenonly the grey matter of the cerebral cortex is used (method2), the odontocetes have a smaller CI than the simians andother mammals used in this analysis. This indicates thatwhile much of the odontocete brain is occupied by thecerebral cortex, as in simians, the amount of grey matterin odontocete (and mysticete) cetaceans is less than thatof simians and other mammals of similar brain sizes.This indicates that a greater proportion of the cerebralcortex of cetaceans is occupied by white matter, whichconnects the various regions of the brain, rather thanby grey matter where neuronal computation occurs. ThisprosimianprimatesCetacean brain evolution and thermogenesis15

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[Show abstract][Hide abstract]ABSTRACT:
Possessing large brains and complex behavioral patterns, cetaceans are believed to be highly intelligent. Their brains, which are the largest in the Animal Kingdom and have enormous gyrification compared with terrestrial mammals, have long been of scientific interest. Few studies, however, report total number of brain cells in cetaceans, and even fewer have used unbiased counting methods. In this study, using stereological methods, we estimated the total number of cells in the neocortex of the long-finned pilot whale (Globicephala melas) brain. For the first time, we show that a species of dolphin has more neocortical neurons than any mammal studied to date including humans. These cell numbers are compared across various mammals with different brain sizes, and the function of possessing many neurons is discussed. We found that the long-finned pilot whale neocortex has approximately 37.2 × 10(9) neurons, which is almost twice as many as humans, and 127 × 10(9) glial cells. Thus, the absolute number of neurons in the human neocortex is not correlated with the superior cognitive abilities of humans (at least compared to cetaceans) as has previously been hypothesized. However, as neuron density in long-finned pilot whales is lower than that in humans, their higher cell number appears to be due to their larger brain. Accordingly, our findings make an important contribution to the ongoing debate over quantitative relationships in the mammalian brain.

[Show abstract][Hide abstract]ABSTRACT:
The present study documents the morphology of neurons in several regions of the neocortex from the bottlenose dolphin (Tursiops truncatus), the North Atlantic minke whale (Balaenoptera acutorostrata), and the humpback whale (Megaptera novaeangliae). Golgi-stained neurons (n = 210) were analyzed in the frontal and temporal neocortex as well as in the primary visual and primary motor areas. Qualitatively, all three species exhibited a diversity of neuronal morphologies, with spiny neurons including typical pyramidal types, similar to those observed in primates and rodents, as well as other spiny neuron types that had more variable morphology and/or orientation. Five neuron types, with a vertical apical dendrite, approximated the general pyramidal neuron morphology (i.e., typical pyramidal, extraverted, magnopyramidal, multiapical, and bitufted neurons), with a predominance of typical and extraverted pyramidal neurons. In what may represent a cetacean morphological apomorphy, both typical pyramidal and magnopyramidal neurons frequently exhibited a tri-tufted variant. In the humpback whale, there were also large, star-like neurons with no discernable apical dendrite. Aspiny bipolar and multipolar interneurons were morphologically consistent with those reported previously in other mammals. Quantitative analyses showed that neuronal size and dendritic extent increased in association with body size and brain mass (bottlenose dolphin < minke whale < humpback whale). The present data thus suggest that certain spiny neuron morphologies may be apomorphies in the neocortex of cetaceans as compared to other mammals and that neuronal dendritic extent covaries with brain and body size.